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Puya Phylogenetics

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Puya Phylogenetics American Journal of Botany 97(2): 337–356. 2010. P HYLOGENETICS OF PUYA (BROMELIACEAE): PLACEMENT, MAJOR LINEAGES, AND EVOLUTION OF CHILEAN SPECIES 1 Rachel Schmidt Jabaily 2 and Kenneth J. Sytsma Department of Botany, University of Wisconsin, Madison, Wisconsin 53706 USA Puya (Bromeliaceae), a large genus of terrestrial bromeliads found throughout a range of elevations in the Andes and central Chile, is of great systematic, evolutionary, and biogeographical interest. This fi rst molecular phylogenetic study of Puya and re- lated bromeliads employs matK , trnS-trnG , rps16 , and PHYC sequences. Chloroplast DNA, nuclear DNA, and combined DNA data all place Puya closest to subfamily Bromelioideae. Nuclear and combined data support Puya as monophyletic, and the two subgenera are nonmonophyletic. All data indicate that the Chilean species of Puya are early diverging within the genus, consistent with Chilean genera as the fi rst-diverging members of subfamily Bromelioideae. Central Chile is identifi ed as a key region for understanding the biogeographical history of Bromeliaceae, as is true with other South American plant groups. A complicated history involving early chloroplast capture and later secondary hybridization and/or introgression is seen in Chilean lineages. These events help explain the occurrence of sterile infl orescence tips, fl oral color and shape, and leaf indument. The ecological radiation of Puya appears coincident with the fi nal, recent rise of the Andes and subsequent high-elevation habitat diversifi cation. Additionally, geographical distribution, rather than moisture or elevational adaptations, correlates to species relationships. Evolu- tion of CAM photosynthesis has occurred multiple times. Key words: Bromeliaceae; Andes; Chile; chloroplast capture; CIPRES; matK , PHYC ; phytochrome C; Puya ; rps16 ; trnS-trnG . Puya , a large genus (ca. 200 spp.; Luther, 2004 ) of terrestrial, The genus Puya was fi rst described by the Chilean priest rosette-leaved bromeliads, is of considerable ecologic, biogeo- G. I. Molina in 1782 and, starting with the treatment of Wittmack graphic, systematic, and evolutionary interest. As one of the (1888) , has always been placed with other bromeliad genera largest radiations in the Bromeliaceae, Puya extends from the with capsular fruits lacking villous seeds. Puya was mono- mountains of Central America, through the mid- to high-eleva- graphed by Lyman Smith as the fi rst group revised in his com- tions of the Andes, and south to lower elevations of central prehensive treatment of Bromeliaceae in Flora Neotropica Chile. In a diversity of both wet and dry habitats, its species ( Smith and Downs, 1974 ). In this defi nitive treatment, Puya exhibit considerable morphological variation in growth form, was placed in the subf. Pitcairnioideae with other genera in- semelparity and iteroparity, infl orescence structure, and fl oral cluding primarily mesic Pitcairnia and primarily xeric Deu- color ( Fig. 1 ). Surprisingly, considering that Puya is one of the terocohnia , Dyckia , and Hechtia . Most other morphology-based most characteristic and recognized elements of the p á ramo and classifi cation schemes placed Puya with Hechtia/Deutero- subp á ramo fl oras ( Luteyn, 1999 ), little is known about phylo- cohnia/Dyckia (among others) apart from Pitcairnia (subtribe genetic relationships of species and evolutionary transitions in Puyinae: Mez, 1896; tribe Puyeae: Mez, 1934 – 1935; tribe Pu- biogeography, habitat, habit, and morphological features. yeae: Varadarajan and Gilmartin, 1988). Thus, phylogenetic Moreover, Puya occupies an important position in the phyloge- relationships among genera comprising subf. Pitcairnioideae netic tree of Bromeliaceae as the putative sister to the large and have long troubled bromeliad systematists, and no classifi ca- diverse subf. Bromelioideae ( Givnish et al., 2007 ; Schulte and tion scheme proposed solely on morphological characters has Zizka, 2008 ). However, sampling of Puya , subfamily Brome- been supported by modern molecular systematic data. The fi rst lioideae and other close relatives has been limited; the exact molecular phylogenies of Bromeliaceae, all using various sin- placement of Puya and composition of its major lineages are gle chloroplast DNA (cpDNA) regions, revealed a broadly pa- unknown. raphyletic subf. Pitcairnioideae ( Terry et al., 1997 ; Horres et al., 2000 ; Crayn et al., 2004 ) and placed Puya as sister to subf. Bromelioideae with fl eshy fruits. The recent molecular phylo- 1 Manuscript received 14 April 2009; revision accepted 24 November 2009. The authors thank R. V á squez, E. Narv á ez, D. Neill, J. Manzanares, M. genetic analysis using ndhF by Givnish et al. (2007) placed the Jabaily, D. Gutierrez, L. Novara, J. Crisci, L. Katinas, M. Rosas, D. Stanton, two sampled Puya as sister to subf. Bromelioideae and this A. Marticorena, M. Diazgranados, D. Rodriguez, N. Anaya, A. Tupayachi, clade as sister to another clade comprising Pitcairnia + ( Deu- M. Nu ñ ez, G. Calatayud, E. Suelli, F. Pela é z, W. Galiano, N. Cano, A. terocohnia , Dyckia , Fosterella , and others), hereafter referred Cano, B. Drew, M. Ames, M. Schmidt, B. Berger, and M. Fernandez for to as subf. Pitcairnioideae. The many morphological similari- help in the fi eld and help with permits; herbaria NY, US, SEL, MO, HNT, ties of Puya with these other xeric genera were argued to be due USZ, LPB, QCNE, LP, MCNS, CONC, COL, USM, CUZ, HUT for letting to convergence ( Givnish et al., 2007 ). Puya was thus placed in the us view specimens; G. Lyons and the Huntington Botanical Garden for newly described and monogeneric subf. Puyoideae ( Givnish et al., supporting work with the living collection; K. Elliot for preparation of the 2007 ). These results have been corroborated by the fi ve cpDNA fi gures; and L. Prince, M. Kinney and C. Pires for help with primers. Laboratory work was supported by NSF grant EF-0431233 (KJS) and an region Bromelioideae phylogeny of Schulte and Zizka (2008) and NSF Graduate Research Fellowship (RSJ). the cpDNA plus low-copy nuclear PRK study of Schulte et al. 2 Author for correspondence (e-mail: [email protected]) (2009) . Recent polyploid events are quite rare in Bromeliaceae and N = 25 has been found for all Puya surveyed ( Smith and Downs, doi:10.3732/ajb.0900107 1974 ; Brown and Gilmartin, 1989 ; Gita í et al., 2005 ). 337 338 American Journal of Botany [Vol. 97 Fig. 1. Representative vegetative and fl oral diversity in both subgenera of Puya and in the Chilean species. Species in left gray box are members of subg. Puya . The remaining photos show species from subg. Puyopsis . Species united by the black line are Chilean Puya species. February 2010] Jabaily and Sytsma — Phylogenetics and evolution in PUYA 339 Puya is found primarily above 1500 m a.s.l. in both moist radiation of Bromelioideae with baccate fruits. Second, Puya and dry habitats from the Cordillera Talamanca of Costa Rica exhibits a remarkable species radiation, involving morphologi- to the dry chaco of Tucum á n, Argentina ( Fig. 2A ). A noticeably cal and ecological variation, along a biogeographical distribu- disjunct group of seven species are found at just above sea level tion from southern Chile to Costa Rica. in central Chile ( Fig. 2B ). This region with a Mediterranean Our aims here are to (1) solidify the placement of Puya in rela- climate represents the southernmost and lowest elevational tion to related subfamilies and genera using greater taxa sampling range of any species of Puya and is separate from the distribu- and additional chloroplast and nuclear gene regions, (2) test the tion of all other Puya by the highest and oldest parts of the monophyly of subg. Puya and Puyopsis , and (3) examine the Andes to the east and the desolate Atacama desert to the north. phylogenetic relationships and morphological evolution of Chil- This region of Chile is also home to all species of Ochagavia ean species in the context of a broader phylogeny of Puya . and Fascicularia and several species of Greigia , three putative early-diverging genera of subf. Bromelioideae ( Horres et al., 2007 ; Schulte and Zizka, 2008 ). Little systematic effort is evi- MATERIALS AND METHODS dent at the infrageneric level within Puya besides the erection of subg. Puya and Puyopsis ( Smith and Downs, 1974 ). The Collections— Fieldwork was conducted from 2006 to 2008 in all major bio- paucity of systematic studies within Puya may be due to two geographical regions where Puya occurs (northern Andes wet p á ramo, northern issues. First, many species are known only from types, and sec- Andean valleys, central Andean puna, central Andean valleys, central coastal Chile). Multiple accessions of several species were taken to test for species ond, obvious characters for morphological comparisons are elu- monophyly, particularly of Chilean species and widespread taxa (e.g., P. rai- sive or are not preserved on most herbarium specimens. Smith mondii and P. ferruginea ). Some samples were taken from the living plant col- and Downs (1974) placed eight species into subg. Puya based lections at the Huntington Botanical Garden (San Marino, California, USA) and on the presence of elongate sterile tips of the compound infl o- Marie Selby Botanical Garden (Sarasota, Florida, USA) (Appendix 1). All rescence, apparently an adaptation to pollination by perching vouchers are deposited at WIS and in home-country herbaria. Forty-three ac- birds ( Johow, 1898 ; Anderson et al., 2005 ). Puya chilensis , P. cessions of Puya are analyzed in this paper, including seven of eight species from subgenus Puya , all species from Chile and a representative sampling of gilmartiniae , P. alpestris , and P. berteroniana are generally re- subgenus Puyopsis encompassing the geographical range of the genus and ma- stricted to central Chile and P. boliviensis is found in a disjunct jor morphological types ( Smith and Downs, 1974 ) ( Table 1 ). Based the recent area further north in Chile. Puya weddelliana is found in xeric molecular phylogenetic results in Bromeliaceae ( Givnish et al., 2007 ), we also southern Bolivia, P. castellanosii occurs in xeric northwest included taxa (for a total of 75 taxa) representing major groups of subf.
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